4

SANTA OLGA CACCIOLA1 AND GAETANO MAGNANO DI

SAN LIO2

MANAGEMENT OF CITRUS DISEASES CAUSED

BY PHYTOPHTHORA SPP.
1
Dipartimento di Chimica Biologica, Chimica medica e Biologia
Molecolare, University of Catania,
Viale Andrea Doria 6, 95126 Catania, Italy
2
Dipartimento di Gestione dei Sistemi Agrari e Forestali, Faculty of
Agriculture, Mediterranean University of Reggio Calabria, 89122 Reggio
Calabria, Italy

Abstract. The complex of citrus diseases caused by Phytophthora spp. is reviewed, with reference to the
damages caused by Phytophtora root rot, gummosis and brown rot of fruits. Some aspects of the biology
and ecology of P. citrophthora and P. nicotianae are revised, like the inoculum dissemination, the fungus
reproduction and epidemiology. The symptomatic diagnosis of main diseases like foot rot or gummosis,
fibrous root rot, brown fruit rot and dieback of twigs and leaves, are reviewed. Biological and
instrumental diagnosis as well as routine laboratory tests are revised, for inoculum monitoring, sampling
and population dynamics procedures. Disease management methods based on interventions on the host-
plant, rootstock resistance, grafting, as well as nurseries sanitary practices are illustrated, together with
pruning, surgery, and cultural practices like soil preparation, fertilization, irrigation and soil management,
and weeds control. Chemical control methods are also reviewed, with reference to the use of systemic
fungicides for control of trunk gummosis, root rot and brown rot of fruits.

1. INTRODUCTION
Citrus are among the ten most important crops in terms of total fruit yield worldwide
(Table 1) and rank first in international fruit trade in terms of value. The term
“citrus” indicates a complex of species belonging to the sub-family Aurantioideae
(family Rutaceae) including the following genera: Citrus, Eremocitrus, Fortunella,
Microcitrus and Poncirus. More than seven million hectares are planted with
citrus throughout the world (Table 2). Although citrus are native to East Asia,
citriculture has expanded in tropical, subtropical and mediterranean climatic
regions (Table 3). Mediterranean countries are the leading producers for the
international fresh market. The all-inclusive term “Phytophthora root rot” indicates a
complex disease which is caused by several soil-borne species of Phytophthora and is
recognized as a major fungal disease of citrus almost universally (Boccas & Laville,
1978; Klotz, 1978; Gregory, 1983; Magnano di San Lio, 1994; Erwin & Ribeiro,

61
A. Ciancio & K. G. Mukerji (eds.), Integrated Management of Diseases Caused by Fungi,
Phytoplasma and Bacteria, 61–84.
© Springer Science+Business Media B.V. 2008
62 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

1996; El-Otmani; 2006; Sadowsky, 2006; Tuset, 2006). Phytophthora spp. attack
citrus plants at all stages and may infect all parts of the tree, including roots, stem,
branches, twigs, leaves and fruits. Root rot, foot rot (also known as “gummosis”,
“trunk gummosis” or “collar rot”), fruit brown rot, twig and leaf dieback (often
indicated collectively as “canopy blight”) and rot (better known as “damping off ”)
of seedlings, all caused by Phytophthora spp., may be considered different facies of
the same disease.

Table 1. Major crops worldwide (FAO, 2004).

Crops Yields (× 1000 tons)

Sugar cane 1,318,178

Mais 705,293
Wheat 624,093
Rice 608,496
Potato 330,518
Sojbean 206,410
Barley 155,115
Sweet potato 127,535
Tomato 124,112
Citrus 108,095

2. DAMAGES CAUSED BY PHYTOPHTORA ROOT ROT

Gummosis and root rot are the most serious facies of Phytophthora root rot. In
nurseries, gummosis can lead to the rapid death of young citrus trees, whereas on
adult trees the disease course is chronic. Usually a mature tree shows symptoms of
decline on the canopy, including leaf chlorosis, philloptosis, dieback of twigs, small
and poor colored fruit, offspring fruit production, twig dieback and withering of
leaves during periods of drought, if the infection affects more than 50% of the
circumference of the trunk.
Root rot is especially harmful if the plant is grafted on a susceptible rootstock.
Young trees are very susceptible. Seriously affected nursery-trees do not overcome
the crisis induced by transplant. The infections on bearing trees cause the decay of
the canopy, defoliation, leaf chlorosis and a reduction in the fruit size and
production. However, plants with a high percentage of infected roots may not show
symptoms. The tolerance to this facies of the disease depends on the capacity of the
plant to regenerate roots and to substitute the rotten ones (Graham, 1995). This
capacity is remarkably reduced if the soil is saturated with water. There are indirect
estimates of the damage caused by this particular aspect of the disease. According to
researches carried out in the United States, the damage in terms of yield losses
 PHYTOPHTHORA MANAGEMENT ON CITRUS 63

caused by root rot is on average about 5%, while the damage caused by gummosis
was estimated to be on average about 1% (Menge & Nemec, 1997).

Table 2. Major citrus producers in the world (FAO, 2004).

Country hectares

China 1,476,679
Brasil 942,267
Nigeria 730,000
Mexico 523,503
U.S.A 430,080
Spain 296,950
India 264,500
Iran 232,500
Italy 168,507
Argentina 145,000
Egypt 143,883
World 7,295,135

Brown rot of fruit is a common preharvest decay of citrus fruit, which causes
the fruit to fall. The infection occurs with rain splash to lower hanging fruits.
Infected fruits picked during the incubation period of the disease can still infect
healthy fruits in storage. This disease causes occasionally severe damage when
heavy or lasting rainfall occurs before harvest.
The epidemic explosions of brown rot usually occur in areas where heavy
rainfall coincides with the early stages of fruit maturity as immature fruits are not
susceptible to the infection. Severe attacks have also been caused occasionally by
overhead sprinkler irrigation, due to the use of water contaminated by Phytophthora
propagules. Annual losses from brown rot vary greatly, even in the same site. As
much as 90% of the crop on an individual tree and up to 30% of the total production
of some orchards were estimated to be lost when the disease was noticed for the first
time in Florida (Knorr, 1956).
Severe damages caused by canopy blight have been occasionally observed in
the nursery and on potted ornamental citrus plants under greenhouse (Kuramoto,
1981; Magnano di San Lio, Tuttobene & Pennisi, 1986; Magnano di San Lio,
Pennisi & Tuttobene, 1986).
Seedling rot is a disease of citrus in nurseries and affects the seedlings just
before or just after they have emerged from soil. It has disastrous effects although
limited in 24 hours, and about 80% of the seedlings in a seedbed may be killed.
64 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

Table 3. Major citrus fruit producers in the world (FAO, 2004).

Country Yields (× 1000 tons)

Brasil 20,594
U.S.A 14,907
China 14,655
Mexico 6,475
Spain 6,206
India 4,750
Iran 3,825
Italy 3,493
Nigeria 3,250
Argentina 2,690
Egypt 2,562
Turkey 2,408
South Africa 1,850
Indonesia 1,600
Pakistan 1,585
Japan 1,470
Greece 1,227
Morocco 1,139
Thailand 1,116
World production 108,181

2.1. Causal Agents

The genus Phytophthora includes about 70 species. It belongs to the family
Pythiaceae, phylum Oomicota, kingdom Chromista or Stramenopila. At least ten
species of Phytophthora, including P. bohemeriae Sawada, P. cactorum (Leb. &
Cohn) Schröeter, P. cinnamomi Rands, P. citricola Sawada, P. citrophthora (R. E.
Smith & E. H. Smith) Leonian, P. hibernalis Carne, P. megasperma Drechsler, P.
nicotianae van Breda de Haan (= P. parasitica Dastur), P. palmivora (Butler)
Butler, and P. syringae Klebahn have been reported to attack citrus in the world.
However, the commonest species of Phytophthora in citrus orchards are P.
citrophthora and P. nicotianae. Other rarer Phytophthora species, such as P.
cactorum, P. citricola, P. hibernalis and P. syringae attack fallen fruits and
sporadically rootlets as well (Favaloro & Sammarco, 1973).
Phytophthora syringae and P. hibernalis, which have a lower optimal
temperature than other species, are found in citrus orchards during winter months.
 PHYTOPHTHORA MANAGEMENT ON CITRUS 65

Phytophthora palmivora is a very polyphagous species of tropical origin and

also attacks citrus orchards. It is very common in Florida (Zitko, Timmer & Sandler,
1991; Graham & Timmer, 2006). In Italy, although it has been found in olive trees,
ornamental plants and garden citrus trees, it did not spread to citrus orchards or to
commercial citrus nurseries (Magnano di San Lio et al., 2002).

2.2. Biology and Ecology

2.2.1. Dissemination and Reproduction

Phytophthora spp. produce various types of propagules: sporangia or conidiangia,
which can germinate directly, through a germ tube, or indirectly releasing zoospores,
motile biflagellate propagules, which lose the flagellum and encyst on contact with
the surface of the host and germinate; chlamydospores, resistant structures which
allow the pathogen to survive in unfavourable conditions; gametangia, called
respectively antheridium (male gametangium) and oogonium (female
gametangium); and oospores, which are formed after sexual reproduction and act
also as organs of preservation. Some species, including P. nicotianae and probably
P. citrophthora, are heterothallic, producing oospores only if the mycelium of the
two different mating types of sexual compatibility (A1 and A2) come into contact
with each other. Natural infections of all parts of citrus are most frequently caused
by zoospores and occasionally by direct germination of sporangia (Klotz & De
Wolfe, 1960).

2.3. Epidemiology
Both P. citrophthora and P. nicotianae are polyphagous, that is, they infect
numerous plant species. Phytophthora nicotianae is more active in warm conditions
than P. citrophthora (Table 4) and attacks mainly the rootlets. P. citrophthora is the
main causal agent of trunk gummosis and fruit brown rot. The primary source of
inoculum is the rhizosphere soil, where the pathogen survives in the roots in the
form of mycelium, chlamydospores and oospores. The infected rootlets and fruits
with brown rot infections are the sources of the secondary inoculum and, in fact,
sporangia are formed on their surfaces, whereas no sporangia are formed on the
gummy cankers at the foot of the trunk. As far as it is known, P. citrophthora does
not reproduce sexually and very probably P. nicotianae reproduces sexually only
occasionally, since in the majority of citrus orchards examined only one mating type
of mycelium is found.
Sporangia are produced on contact with air on the most superficial soil layers
and are transported on the fruits by rain, irrigation water and wind. They germinate
in water, and a single sporangium releases from 5 to 40 zoospores. Production and
germination of sporangia are influenced above all by temperature and soil water
potential. The zoospores are motile and can swim short distances by flagellar
movement or can be carried over longer distances by soil water. The zoospores are
attracted by root exudates and sweem towards roots and encyst upon contact. Cysts
66 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

then germinate and penetrate the cortex through wounds or directly. The zoospores
can affect any part of the plant, if it remains wet at least 18 hours. The trunk,
branches and roots are infected through lesions, but the zoospores germ tube can
penetrate fruits, leaves, shoots and green twigs directly even in absence of lesions.

Table 4. Cardinal temperatures (°C) for mycelium growth of citrus

isolates of Phytophthora citrophthora and P. nicotianae.

Minimum Optimum Maximum

P. citrophthora 5 25-28 35
P. nicotianae 5-10 28-30 35-38

Soils rich in calcium have a repressive effect on Phytophthora populations

(Campanella, Ippolito & Nigro, 2002), whereas the amounts of NaCl accumulated in
soil after using saline irrigation water may stimulate the production of sporangia.
NaCl may also damage the roots, increasing their susceptibility to infection (Blaker
& MacDonald, 1985). In general, host susceptibility is affected when roots are
stressed or damaged, and root exudates released by damaged or stressed roots attract
zoospores (Graham & Timmer, 2006).
Temperature is a major ecological factor affecting the seasonal fluctuations of
P. citrophthora and P. nicotianae and their distribution. In the Mediterranean region
P. nicotianae is not active in winter, while P. citrophthora is not inhibited by winter
temperatures (Timmer et al., 1989; Ippolito, De Cicco & Salerno, 1992).
Conversely, the activity of this latter species is dramatically reduced in hot summer
months with the exception of short periods following irrigation (Magnano di San Lio
et al., 1988; 1990).
Phytophthora nicotianae is more common in subtropical areas and causes foot
and root rot. Occasionally it attacks aerial parts of the tree causing brown rot of
fruits, but usually it does not infect far above the ground. Phytophthora citrophthora
causes brown rot outbreaks during fall and winter. In subtropical areas this species is
restricted to cooler weather sites and coastal areas (Feld, Menge & Pehrson, 1979).
However, as both species may grow and reproduce between 15 and 30 °C, the range
of soil temperature of most citrus orchards throughout the year, it appears unlikely
that summer soil temperatures may result sufficient to inhibit P. citrophthora.
There is evidence that Phytophthora inoculum fluctuations are strongly
influenced by the physiological conditions of the host-plant, which in turn are
correlated with temperature. Seasonal variations of citrus trees physiology, for
example, are a major factor determining the susceptibility of fibrous roots to the rot
incited by P. nicotianae (Lutz & Menge, 1991; Matheron & Matejka, 1993).
Summer activity of this species is directly correlated with both the production of
root exudates and the concentration of sugars in the roots, but it is inversely
 PHYTOPHTHORA MANAGEMENT ON CITRUS 67

correlated with starch concentration (Fig.1). Also the bark susceptibility to infection
by P. citrophthora in subtropical and mediterranean climates varies throughout the
year and is higher in spring and autumn and very low in winter and summer
(Matheron & Matejka, 1989; Adonia et al., 1992).
In subtropical and mediterranean areas, when soil temperature falls to about
12°C, citrus roots stop their growth. In these circumstances, P. nicotianae forms
chlamydospores and becomes inactive. The subsequent population increase of this
species occurs in spring, when soil temperatures rise again, and coincides with a
new flush of roots. In tropical regions, where roots grow almost all the year,
seasonal fluctuations of plants susceptibility to root rot infections are less evident.
Phytophthora palmivora is found in tropical areas but its epidemiology is more
similar to that of P. citrophthora. It attacks preferentially fibrous roots and fruit. The
fruit is susceptible to brown rot infections from the ripening phase.
Brown rot epidemics are more frequent in citrus orchards where trunk gummosis
is endemic. If the environmental conditions are favourable for infections, for instance
when there is heavy rainfall in the winter period, brown rot is associated with the
dieback of leaves and twigs. The incubation period of brown rot is 3 – 7 days,
according to the temperature (Schiffmann-Nadal & Cohen, 1966). Asymptomatic
infected fruits can still infect healthy fruits even after harvesting, during transportation
and storage.

2.4. Symptomatic Diagnosis

2.4.1. Foot Rot or Gummosis

The specific symptoms of this facies of the disease are the cankers and gummosis at
the base of the trunk (Fawcett, 1936). Gum oozes proceed from longitudinal cracks
of the bark around necrotic areas, which have a distinct water-soaked discoloration.
The dead bark turns soft and sloughs off the central cylinder below which a callous
is formed around the edges of the lesion. If the canker affects more than 50% of the
trunk circumference, the plant shows symptoms of decline in the canopy, chlorosis
of the veins and also midrib of the leaf, philloptosis, thinning of the canopy and
dieback of branches. Gum exudation can be seen on trees especially between the end
of spring and beginning of summer. The gum is water-soluble, but even if it is
washed away by the rain, the discolouration on the cortex is still visible. Since the
cankers are often formed below ground, it may be necessary to scrape away the soil
around the collar to see them and evaluate the severity of infection.

2.4.2. Fibrous Root Rot

This is the most difficult facies to diagnose by visual inspection, since similar
symptoms can be caused by different factors, like poor soil aeration and excessive
salt content in irrigation water (Klotz et al., 1958). The root cortex sloughs off
easily, leaving the stele bare, with the tip of the rootlet appearing thread-like. The
plant reacts to the infection by forming new rootlets. Adult plants may show no
symptoms even when there is a very high percentage of infected rootlets. The
68 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

symptoms of decay on the canopy appear when the plant is no longer capable of
producing new rootlets to substitute the rotten ones.

2.4.3. Brown Fruit Rot and Dieback of Twigs and Leaves

Infected fruit show a leathery brown rot with indistinct edges and have characteristic
rancid odour (Feld, Menge & Pehrson, 1979). If the humidity in the air is high,
white furry mould can be seen on the fruit surface. In environmental conditions
especially favourable to brown rot of fruits, symptoms can also be observed on
leaves and twigs. Infected leaves show dark brown oil-soaked necrotic spots with
indefinite margins, dry up and fall early. These necrotic lesions appear frequently on
the leaf tip. The infected twigs show gummosis, browning of the cortex, defoliation
and dessication.

2.5. Biological and Instrumental Diagnosis

2.5.1. Baits
In citrus orchards, the presence and quantity of Phytophthora inoculum in soil can
be determined empirically according to how frequently the ripe fruit left on the
ground for 3 – 7 days is infected. Ripe fruit of lemon and sweet orange can be used
as bait to capture P. citrophthora in the soil. Fragments of leaves from different
citrus cultivars are universal baits, i. e. they can be used to capture all Phytophthora
species living in citrus orchards. About ten grams of soil are incubated at ambient
temperature in the dark in a paper-glass filled with distilled water (soil : water ratio
1:6). After 4-6 days of incubation leaf pieces are picked up and observed at the
microscope for the presence of sporangia along the leaf cut edge. Another option is
to transfer the leaf fragments used as baits in Petri dishes on a selective isolation
medium and to identify the Phytophthora colonies grown from baits after 3-6 days
of incubation at 22-24 °C (Magnano di San Lio & Perrotta, 1982). However, to
identify the species or to determine the exact amount of inoculum, laboratory tests
are required.

2.5.2. Laboratory Analysis

In routine laboratory tests to obtain axenic cultures of Phytophthora from soil or
rotten tissues, isolation on selective media, such as BNPRAH or PARP (Erwin &
Ribeiro, 1996), is the most frequently used microbiological method. Similarly, serial
dilution of soil aliquots in Petri dishes on a selective medium is a very popular
method to determine the quantity of inoculum in soil. Diagnostic kits based on the
double-antibody-sandwich-enzyme-linked immunosorbent assay (DAS-ELISA) with
genus-specific polyclonal and monoclonal antibodies have been developed for
detection of Phytophthora spp. in roots and soil debris (Pscheidt et al., 1992;
Cacciola, Pennisi & Magnano di San Lio, 1995).
 PHYTOPHTHORA MANAGEMENT ON CITRUS 69

Although the ELISA method is highly sensitive and can detect the presence of
Phytophthora at lower population densities than dilution plating onto selective
media (Timmer et al., 1993), it has not been applied on a large scale for
Phytophthora detection in citrus orchard, probably because of the special laboratory
equipment which is needed to obtain quantitative data.
Molecular detection methods have been developed more recently, including
PCR with species-specific primers, nested-PCR with genus and species-specific
primers as well as real time-PCR (Ippolito, Schena & Nigro, 2002; Grote et al.,
2002; Ippolito et al., 2004). The molecular methods are very sensitive and rapid but
may be applied in specialised laboratories only.

2.5.3. Monitoring of Inoculum

2.5.3.1. Definition
Monitoring consists in periodically determining the quantity of inoculum of the
various species of Phytophthora present in the soil of the citrus orchard or in the
irrigation water. Quantitative methods are used, such as isolation from infected
organic material (roots, leaves, bark etc.) on selective media, insemination of the
substrate with a series of soil dilutions, the DSA-ELISA assay on infected roots or
molecular analysis using Real time-PCR of the DNA extracted from samples of
water, soil or organic material. Monitoring is useful, especially for the rational
timing and management of chemical treatments (Sandler et al., 1989; Matheron
Porchas & Matejka, 1997).

2.5.3.2. Critical Values of Inoculum Density

The quantity of inoculum determined with microbiological methods is generally
indicated as inoculum density (ID) and is expressed in terms of Colony Forming
Units (CFU) / g or cm3 of soil or water. The ID critical values in soil (also defined
threshold or danger levels) have been determined experimentally and can be used to
evaluate the effects of control options or as a guideline to program treatments. The
threshold intervention level in bearing orchards is 10-20 CFU/cm3 of soil (Magnano
di San Lio, Tuttobene & Perrotta, 1984; Menge, 1986; Timmer et al., 1988), but for
newly transplanted plants or for nursery stock it might be 3-5 CFU/cm3 (Magnano di
San Lio, Tuttobene & Perrotta, 1984; Magnano di San Lio et al., 2002).
The ID of P. nicotianae is directly related to the mass of fibrous roots, as
infected roots provide substrate for the propagules multiplication (Agostini, Timmer
& Castle, 1991; Sandler et al., 1989). Thus population levels of this species
generally diminish with soil depth and with distance from the tree. Highest
population densities of P. citrophthora (more than 100 CFU/cm3) have been found
in soil of citrus orchards during epidemic explosions of fruit brown rot (Magnano di
San Lio et al., 1988). Usually, however, in most citrus orchards ID values range
from 1 to 20 CFU/cm3.
70 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

Population levels show a seasonal pattern (Fig. 1) and may vary considerably
from year to year. It is also important to remind that Phytophthora populations in
soil are not uniform across the orchard. Studies on their horizontal spatial
distribution indicate either a random or an aggregate negative binomial pattern
(Magnano di San Lio, Reforgiato & Russo, 1987; Timmer et al., 1988; Magnano di
San Lio & Pennisi, 1994; Graham & Timmer, 2006). Because of this not uniform
spatial pattern of the inoculum, a great number of soil samples might be required to
detect lowest ID. Timmer et al. (1988) suggested that Elliot’s equation may be used
to calculate the number of soil samples theoretically needed to obtain a reliable
estimate of the ID of Phytophthora populations, fitting a negative binomial
distribution. They estimated that about 5-10 samples/hectare would be sufficient to
determine the mean ID in citrus orchards with moderate to high inoculum level.

2.5.3.3. Sampling
The criteria suggested in practice for collecting soil samples to determine routinely
ID are the following: the soil samples are taken from the rhizospere of the tree at a
depth of about 10-30 cm, under the tree canopy in the area soaked by irrigation
water, and they must contain rootlets. Each sample is obtained by mixing 20-40 sub-
samples taken from at least 4 trees over a surface of about 4 hectares, to give an
overall weight of 0.5-1 kg. It is advisable to analyse the sample within 24-48 hours
after its collection. If it must be kept for a longer period, it should be stored at room
temperature in a plastic bag, which should be left open to avoid water condensation.

Figure 1. Schematic representation of seasonal patterns of populations of Phytophthora

citrophthora and P. nicotianae in soil of citrus orchards in Mediterranean climate and
relationship between inoculum density, expressed as colony forming units (CFU) · gram of
soil-1, and physiological parameters of citrus trees.
 PHYTOPHTHORA MANAGEMENT ON CITRUS 71

2.5.3.4. Population Dynamics

The best period of the year to collect soil samples is determined by the seasonal
fluctuations of the quantity of inoculum of the two main Phytophthora species
present. Generally speaking, the ID values of P. citrophthora are highest in spring
and autumn, whereas those of P. nicotianae in summer months (Fig 1). In summer
P. citrophthora rarely can be isolated from soil, while P. nicotianae is dormant
during the winter months. As a rule, if it is not clear which Phytophthora species is
prevalent in the citrus orchard soil, the best time to take samples is between March
and November, 1-2 days after irrigation.

2.5.3.5. Molecular Methods

When applying molecular methods for the quantitative determination of the
inoculum, it has been shown that a direct correlation occurs between the ID values
determined by isolation on selective substrates and expressed in terms of CFU and
the quantitative analysis values of DNA determined by Real time-PCR (Ippolito
et al., 2004).

3. DISEASE MANAGEMENT

Disease management mainly relies on the deployment of some specific interventions

on the host-plant, including the selection and use of resistant rootstocks, grafting,
and further sanitary practices applied since the early plant growth phases in citrus
nurseries. Pruning and plant surgery may also be applied as routine practices.
Further phytosanitary practices include soil preparation, irrigation management,
fertilising, soil management and weeds control. Finally, chemical control is
considered, through the application of fungicides with different modes of action.
3.1. Interventions on the Host-Plant
3.1.1. Rootstock
One of the main factors on which incidence, intensity and spreading of the foot and
root rot infections depend is given by the rootstock degree of susceptibility.
Resistance to Phytophthora root rot, therefore, is one of the characteristics to be
taken into account when selecting a rootstock (Table 5).
Since the epidemic outbreaks of the 1860s in the Mediterranean area, the
control of Phytophthora foot and root rot has been mainly based on the use of
resistant rootstocks (Magnano di San Lio, 1994; de Franqueville, 2002). In Japan,
for example, foot rot is considered a minor disease thanks to the widespread use of
trifoliate orange, Poncirus trifoliata (L.) Raf., as rootstock (Kuramoto, 1981).
Although the use of resistant plants is one of the best and most practical means
to control Phytophthora root rot, some rootstocks resistant to Phytophthora are
susceptible to other diseases or are horticulturally unsatisfactory (Ferguson,
Sakovich & Roose, 1990). The rootstocks resistant to P. citrophthora infections are
72 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

also resistant to P. nicotianae. However, it is not always true that a rootstock

resistant to foot rot is also resistant to root rot. For example, sour orange (C.
aurantium L.) and “Carrizo” citrange (C. sinensis Osbeck × P. trifoliata [L.] Raf.)
are tolerant to foot rot but are susceptible to root rot (Graham & Timmer, 2006).
Trifoliate orange is resistant to both foot and root rot.

3.1.2. Grafting
The bud union must be enough far from ground level (above or at least 40 cm) to
prevent the Phytophthora inoculum present in soil from reaching the scion through
water splashing (Whiteside, 1972). Most of the citrus species and cultivars used as
scions, in fact, are susceptible to Phytophthora infections. Grafting with highly
susceptible species or cultivars such as clementines or nucellar clones of sweet
orange may reduce rootstock resistance (Boccas & Laville, 1978; Laville, 1984;
Feichtenberger et al., 1994; Ippolito et al., 1994; Ippolito, Nigro & Lima, 1997).

3.1.3. Sanitary Practices in Nurseries

The inoculum found in bearing orchards usually comes from the nursery. Ideally,
when a new citrus orchard is planted, the plantlets must be free of Phytophthora
infections. This is reccomended in countries that have introduced certification
schemes for nursery citrus plants. The plants with symptoms of gummosis on the
trunk must be eliminated before planting. If a high percentage of plants in a nursery
show symptoms of gummosis or the mean value of Phytophthora ID in the
rhizosphere soil is above 3-5 CFU/cm3, it would be advisable to discard the whole
lot. Management of seedling damping off is based on prevention by using seeds
extracted from healthy fruit and dressed with fungicides, then sowing them in
sterilised soil and irrigating with non-contaminated water. Other sanitary
recommendetions in citrus nurseries can be summarised as follows:

- soil fumigation with i.e. Vapam or sterilisation with steam, before planting;
- limit as far as possible the transit of people or vehicles in the nursery;
- grow plants in separated containers;
- keep the containers above ground level on benches or gravel beds
- avoid resting containers on water-proof plastic sheets, tarmac or cement;
- examine the plants periodically and eliminate those with symptoms of
gummosis to prevent the disease from spreading;
- do at least one quantitative determination of the Phytophthora inoculum
density in the soil of the containers between April and November;
- do not excede with irrigation;
- select a nursery site at some distance from commercial citrus orchards;
- avoid using machinery and tools previously used in other citrus orchards.
PHYTOPHTHORA MANAGEMENT ON CITRUS 73
74 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

3.1.4. Pruning
Pruning modifies the architecture of a tree and may have an effect on the diseases
caused by Phytophthora. For example, the removal or the thinning of the lower
branches can create an unfavourable habitat for trunk gummosis infections and
reduce the risk of infections of fruit brown rot. Drastic pruning or topworking of
plants with symptoms of decline due to foot or root rot reduce the volume of the
canopy and prevent the tree from collapsing. Moreover, it helps the tree to recover,
given the predisposing causes of infection are removed, and will result in a more
efficient management if complemented by chemical treatments.

3.1.5. Surgery
Surgical intervention, practised in the past before systemic fungicides were
introduced to help infected plants recover from foot gummosis (Klotz, 1978), is now
almost obsolete. This is indeed a laborious and time consuming practice. It consists
in carving out the rotten bark. There must be a clean cut to help the scar to cicatrize
quickly and it is not necessary to penetrate too deeply into the woody cylinder. The
lesion can be disinfected with copper-based products, such as the Bordeaux mixture,
copper oxychlorides or mixtures of systemic copper-based fungicides. An alternative
method could be to cauterise the gummy canker with a flame, without removing the
bark (an ordinary blowtorch can be used).

3.2. Cultural Practices

3.2.1. Soil Preparation
An accurate preparation of the planting site, including 80-100 cm deep ditch before
the planting, underground drainage and a superficial soil levelling to allow rainwater
to run off and drain away, prevent stagnation and consequent water saturation of the
soil. Water saturation is one of the main predisposing factors for Phytophthora
infections. When a site has to be replanted, a period of 6-12 months fallowing will
effectively reduce Phytophthora populations as well as other soilborne pests such as
citrus nematode. The young trees must be planted at the same depth as in the nursery
to avoid burying the collar. Putting soil in raised beds (also named mounding or
“meseta” in Spanish), to avoid burying the collar and soil waterlogging under the
tree canopy where the root density is higher, is an example of prevention based on
soil management. This type of soil preparation is especially used and popular where
citrus orchards are planted in heavy soils (El-Otmani, 2006; Schillaci et al., 2006).

3.2.2. Irrigation Management

A fundamental part of the life cycle of P. citropthora and P. nicotianae is spent in
water. The sporangia release zoospores if the soil or the atmosphere is saturated with
water. The released zoospores reach their targets (i.e. the roots, trunk, fruit, branches
or leaves) through water. Finally, an essential condition for the infection to take
 PHYTOPHTHORA MANAGEMENT ON CITRUS 75

place occurs when the host surface remains moist for some hours (at least 18),
giving enough time for the zoospores to germinate and for the germ tube to
penetrate. Another aspect to consider is that hypoxia, which is a consequence of the
soil water saturation, increases the susceptibility of citrus trees roots to
Phytophthora infections and inhibits the growth of new roots.
From this epidemiological knowledge it is convenient to follow some simple
general principles for rational irrigation management:
a) use water not contaminated by Phytophthora;
b) do not wet the trunk;
c) avoid flooding the soil.
Irrigation methods that wet the trunk favour gummosis infections. When one of
these methods is used, it is preferable to irrigate during the day and for short periods,
in order to allow water to evaporate and reduce the time the bark remains wet. As a
root rot preventive practice, the time intervals between irrigations can be extended
(Ohr & Menge, 2006) to reduce the water potential of the upper layers of soil below
the lowest values for P. citrophthora and P. nicotianae activity (Fig. 2). By this
way, the ID in the soil layers with the higher concentration of roots is reduced.
However, the practical application of this concept is difficult. In a study aimed at
determining the influence of different irrigation regimes on Phytophthora rot of
feeder roots, it was shown that in the presence of Phytophthora spp. larger plants
with healthier roots were obtained with frequent irrigation scheduled on the basis of
tensiometer readings, thus suggesting that the practice of drying out orchards soils to
reduce root rot problems is unnecessary, unless excess water was added to soil
(Stolzy, 1959). In the case of irrigation water, it is important to avoid premature
irrigations in spring, when roots are inactive. A recommended practice would be
irrigations of shorter duration with the frequency adjusted on instrument readings
(Ohr & Menge, 2006).
Generally speaking, the use of localised irrigation methods, such as drippers,
makes the plants more vulnerable to root rot. In fact, the ID of P. nicotianae is
directly correlated to the root density which, in arid or semi-arid environments, is
inversely proportional to the volume of soil wetted by irrigation water. In citrus
orchards irrigated in this way, constant monitoring of the water status using
tensiometers is recommended to avoid soil saturation. The effect of various methods
of irrigation on soil populations of Phytophthora has also been investigated by many
authors (Magnano di San Lio et al., 1988; Feld, Menge & Stolzy, 1990; Ippolito,
Lima & Nigro, 1992).

3.2.3. Fertilising
In citrus orchards with problems of root rot, it is better to apply nitrogen in nitrate
rather than ammonium form. The ammonium nitrogen, in fact, is rapidly
metabolised to asparagine and glutamine. These amino acids provide ideal
nourishment for P. nicotianae and attract zoospores (Menge & Nemec, 1997).
76 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

Figure 2. Effect of soil water status on the epidemiology of Phytophthora

citrophthora and P. nicotianae.

3.2.4. Soil Management and Weeds Control

Removing the soil around the collar creates unfavourable conditions for gummosis
infections, since it prevents the bark at the foot of the trunk from remaining moist
for too long, and helps the cankers to heal. Vice versa, the development of weeds
around the collar creates a favourable habitat for gummosis infections, since it
prevents the quick drying of the bark.
The use of herbicides is a way of removing this problem and makes periodic
inspections to detect gummosis infections and their treatment easier. The use of
herbicides on the row, moreover, reduces the risk of wounds on the trunk, which
provide entry points for infection. The lesions, before healing, are prone to
infections for about two weeks (Graham & Timmer, 2006).
Mechanical tilling of the soil near the trunk leads to burying the base of these
trunk, causes lesions and therefore aids collar gummosis infections. Deep tilling aids
root rot since it damages the roots, making them susceptible to infections. Grass
growing between the rows during the winter months reduces the risk of epidemic
explosions of brown rot since it softens the impact of the rain on soil. It also
 PHYTOPHTHORA MANAGEMENT ON CITRUS 77

prevents the inoculum present in soil from coming into contact with fruits and
leaves, trough water splashing.

3.3. Chemical Control

3.3.1. Systemic Fungicides

Control by chemical means is a widespread practice, especially since very effective
systemic fungicides like metalaxyl and Al ethyl-phosphyte (or fosetyl-Al) were
made available (Farih et al., 1981; Davis, 1982; Timmer & Castle, 1985). More
recently, metalaxyl was substituted by its enantiomer metalaxyl-M (or mefenoxam)
which is effective at a lower dosage. Another derivate of phosphorous acid,
potassium phosphonate, which is on the market as fertiliser, acts in the same way as
Al ethylphosphite (Walker, 1988; Adonia et al., 1992; Tuset, Lapena & Garcia-
Mina, 2003). On the whole, these fungicides are effective against both P.
citrophthora and P. nicotianae.
However, there are slight differences in their range of action: fosetyl-Al is
slightly more effective against P. citrophthora, whereas mefenoxam is more
effective against P. nicotianae. The derivates of phosporous acid are translocated up
and down in the plant so they can be applied to roots, trunk or leaves. Their
application is recommended in a preventive way, to trees that are still apparently
healthy or slightly infected and during periods of plant intensive physiological
activity. Mefenoxam only moves upwards and must be applied to the ground or to
the bark to be effective. Both groups of fungicides will remain active in the plant
tissues for 3-4 months (Matheron & Matejka, 1988). Mefenoxam has a toxic action
directly on mycelium growth and on the sporulation of the two species of
Phytophthora. The activity of the phosphorous acid derivates, on the other hand,
depends mainly on their capacity to trigger off the defence mechanisms of the plants
based on the production of phytoalexins and, to a lesser degree, on inhibiting the
development of the pathogen (Afek & Sztejnberg, 1988).
Recently, a new systemic fungicide, dimetomorph, applied as trunk paint at high
concentrations proved to be as effective as fosetyl-Al and mefenoxam in suppressing
canker development on citrus bark, after inoculation with P. citrophthora and P.
nicotianae (Matheron & Porchas, 2002). Other systemic fungicides active against
Oomycetes are being testing and evaluating for a possible use against Phytophthora
diseases of citrus. Some of these compounds appear promising and showed the ability
to inhibit gummosis when applied as foliar spray on citrus plants artificially inoculated
with P. citrophthora at various time intervals after the treatment (Fig. 3). Moreover,
like fosetyl-Al and mefenoxam, these new fungicides showed a long-lasting preventive
activity (Cacciola et al., 2007). Figure 3 e.g. shows that fosetyl-Al, applied as reference
product, and product A (new a. i.) were systemic and showed a long-lasting preventive
activity. Foliar spray with these two fungicides 49, 35, 21 and 7 days as well as 24
hours before inoculation inhibited canker development on twigs as well as on the basal
part of the stem. Product B (a new dipeptide fungicide) was less effective and
persistent. Inhibition of canker on scion twigs and basal stem of the rootstock was
significant only in trees treated 24 hours before inoculation.
78 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

Figure 3. Effect of three systemic fungicides, applied as foliar spray (175 g a.i. ·100 liter -1
H2O) at various time intervals before inoculation with Phytophthora citrophthora, on the
development of cankers on sweet orange trees grafted on sour orange. A) Effect of
treatments on the length of cankers on the twigs (sweet orange), 21 days after
inoculation. B) Effect of treatments on cankers size on the basal portion of the rootstock
stem (sour orange), 70 days after inoculation (mean of 8 replicates ± SE).

3.3.1.1. Trunk Gummosis

To control this facies of the disease, mefenoxam can be applied to the plant through
trunk painting or through the ground. The phosphorous acid derivates are applied via
the leaves. They are effective also as trunk paints. Painting and spraying the trunk
 PHYTOPHTHORA MANAGEMENT ON CITRUS 79

with high concentrations of these fungicides (6% a.i. of mefenoxam and 10% a. i. of
fosetyl-Al) also help the plant to recover. The treatment must be started at the first
sign of symptoms and must be repeated after 3-4 months. If more than 50% of the
tree circumference is affected by gummosis, then the treatment is no longer effective
and it is better to substitute the plant. Painting and spraying of the trunk can also be
carried out using copper-based products, but this has only a preventative effect,
since these products do not penetrate the bark. Painting is impractical if trunk
infection is under the soil level.

3.3.1.2. Root Rot

To control this facies of the disease, both mefenoxam and fosetyl-Al can be used in
the ground. However, fosetyl-Al and the other phosphorous acid derivates are more
effective when applied as foliar spray. In young plants the treatment must be applied
routinely for the first 2 years since the young citrus seedlings are highly susceptible
to root rot. In bearing citrus orchards the treatment should be applied when at least
one of the following premises is met:
- the trees are grafted on a susceptible rootstock;
- the citrus orchard is on a site where root rot is chronically present because
of environmental conditions which cannot be modified;
- the ID values of Phytophthora in the rhizosphere soil reach a critical level
around 15-20 CFU / g or cm3 of soil (lower values can also be considered
critical if the Phytophthora population is made up mainly of P.
citrophthora, or if the rootstock or scion - rootstock combination is highly
susceptible).
It is advisable to apply mefenoxam through the irrigation system, if localised .
To avoid being washed away, the fungicide must be distributed at the end of the
irrigation cycle. In some soils mefenoxam may be degraded quickly by the bacterial
population in the soil (14-28 days) (Bailey & Coffey, 1985). However, if the product
is applied through an irrigation system, it may be absorbed in 2-9 days. Another way
of safeguarding against biodegradation in soil is to alternate applications with foliar
treatment of phosphorous acid derivates, in order to reduce selective pressure on the
microbial populations in the ground. This alternation of active principles also helps
to prevent phenomena of resistance to mefenoxam in the Phytophthora populations.
Treatments against foot and root rot using systemic fungicides protect the fruit
from brown rot infections in both the pre- and post-harvest phases. The treatments
must be timed according to the population dynamics of the pathogenic agents and
the physiological state of the plant.
In the case of root rot caused by P. nicotianae the most suitable period for
treatment is immediately before roots begin to develop, when the first spring growth
flush is three quarters of maximum. The treatment should be repeated in summer. If
root infections are caused by P. citrophthora and are associated with foot rot, the
applications should also be repeated in autumn before winter rains and plant
dormancy or by the end of winter, a few weeks before the spring foliage flush. Even
80 S. O. CACCIOLA AND G. MAGNANO DI SAN LIO

in this case a second application may be necessary in summer. Since both

mefenoxam and phosphorous acid derivates are systemic, applications must be
timed well in order to obtain a high concentration of fungicide in the trunk bark and
in the roots when the plants are most susceptible to infection.

3.3.1.3. Brown Rot of Fruit

The risk of epidemic explosions of brown rot of fruit is greater in citrus orchards
where there is a high incidence of foot and root rot caused by P. citrophthora. To
control this facies of the disease in the field, the canopy is preventatively treated
with phosphorous acid derivates or copper-based products. Some commercial
formulations of copper fungicides are not coloured purposely in order not to stain
the fruit close to harvest. The most suitable time for treatment is before the winter
rains, generally by the first week of November and if the winter is especially wet, a
second application in January-February is recommended.

4. CONCLUSIONS
Research on the ecology and epidemiology of P. citrophthora and P. nicotianae has
provided a corpus of knowledge and data which has been essential for the
development of rational strategies of integrated management of Phytophthora root
rot in citrus orchards and nurseries. These strategies are based on concepts, such as
inoculum density, threshold levels, host susceptibility and pathogen population
dynamics, as well as on general principles, such as use of genetic resistance of the
host, monitoring of inoculun, reduction of inoculum potential, timing of treatments,
sanitation measures, management of cultural practices to obtain an environment less
favourable to the pathogen and to reduce the disease pressure, induction of
resistance and eradication of infections by chemicals.
The efficacy of fosetyl-Al and mefenoxam has relaunched chemical control as
essential part of a rational and effective management strategy of this complex
disease. Proper timing and mode of application of these fungicides based on the
knowledge of the type of fungicide activity, the dynamics of pathogen populations
and the seasonal fluctuations of host susceptibility can help in reducing the
environmental impact of chemicals. The introduction in the scenario of new
systemic active ingredients adds flexibility to the chemical control and can help in
reducing the potential rik of fungicide resistance in the patogen populations.
The substitution of a resistant rootstock such as sour orange, due to further
spread of Citrus Tristeza Virus in the Mediterranean area and the diffusion of
cultivars, such as clementine and nucellar clones of sweet orange (Laville 1984,
Ippolito, Nigro & Lima, 1997), which induce susceptibility even in a tolerant
rootstock, might encourage the use of fungicides as routine control methods.
However, to be effective chemical control of Phytophthora root rot must be
complemented by cultural practices in order to make the environment less
favourable for infections and to reduce the disease pressure.
Genetic resistance of the rootstock appeared to be the most effective means to
control Phytophthora gummosis since the devastating epidemics of the second half
 PHYTOPHTHORA MANAGEMENT ON CITRUS 81

of the 19th century. There is evidence that in the Phytophthora-citrus pathosystem

both olygogenic and polygenic types of resistance are involved (Laville, 1975)
suggesting that it is advisable to select new resistant rootstocks from hybrid
populations obtained by interspecific crosses (de Franqueville, 2001). Phytophthora
root rot of citrus, like other tree diseases, is characterised by a high potential
variability of the pathogen, a low variability of the host and a strong selection
pressure on pathogen populations. Using a polygenic horizontal resistance ensures
durability and efficacy in different geographic areas.

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